Acta Physiologiae Plantarum

, 40:210 | Cite as

Exogenous 5-aminolevulinic acid pretreatment ameliorates oxidative stress triggered by low-temperature stress of Solanum lycopersicum

  • Tao Liu
  • Jiaojiao Xu
  • Jiao Zhang
  • Jianming LiEmail author
  • Xiaohui HuEmail author
Original Article


Low temperature is an important limiting factor in tomato production in early spring and winter. 5-Aminolevulinic acid (ALA) protects crops against varied abiotic stresses. However, the methodology to precisely use ALA to increase the cold tolerance in tomatoes is still not fully known. We therefore explored the effects of ALA concentration, application period, and dose on membrane lipid peroxidation, antioxidation, photosynthesis, and plant growth in different tomato cultivars (Zhongza No. 9, ZZ and Jinpeng No. 1, JP) at low-temperature stress. Results revealed that low temperature caused plants oxidative damage and growth inhibition in both ZZ and JP plants. The ROS (hydrogen peroxide and superoxide anion) accumulation and membrane lipid peroxidation (malondialdehyde content and the relative electrical conductivity) were more remarkable in JP plants than ZZ plants under low temperature. The catalase (CAT) and ascorbate–glutathione cycle (AsA–GSH) induced by ALA reliably eliminated excessive ROS to maintain the redox balance in both tomato cultivars under low-temperature stress. In AsA–GSH cycle, AsA regeneration was mainly catalyzed by dehydroascorbate reductase (DHAR) and monodehydroascorbate reductase (MDHAR), from dehydroascorbate (DHA) to AsA and monodehydroascorbate (MDA) to AsA in ZZ plants, while AsA regeneration in JP plants was mostly catalyzed by DHAR, from DHA to AsA. The ALA optimum concentration was 25 mg L−1. The tomato plants with five true leaves pretreated with 6 mL ALA were more effective than spraying after cold occurred. In conclusion, the two tomato varieties illustrated different capacities to bear low-temperature stress. And ZZ plants were more tolerant to low temperature than JP plants. Precise ALA pretreatment observably alleviated low temperature induced-damage via CAT and AsA–GSH cycle in both cultivars. The regeneration of AsA in AsA–GSH cycle may be more comprehensive in ZZ plants than JP plants, to better tolerate low-temperature stress.


5-Aminolevulinic acid Tomato Low temperature Concentration Dose Spray period 



This work was supported by the National High-tech R&D Program of China (863 Program) (2013AA103004), the China Agriculture Research System (CARS-23-C-05) and the National Natural Science Foundation of China (31772359).


  1. Akram NA, Ashraf M (2013) Regulation in plant stress tolerance by a potential plant growth regulator, 5-aminolevulinic acid. J Plant Growth Regul 32:663–679CrossRefGoogle Scholar
  2. Ali B, Xu X, Gill RA, Yang S, Ali S, Tahir M, Zhou WJ (2014) Promotive role of 5-aminolevulinic acid on mineral nutrients and antioxidative defense system under lead toxicity in Brassica napus. Ind Crop Prod 52:617–626CrossRefGoogle Scholar
  3. An YY, Li J, Duan CH, Liu LB, Sun YP, Cao RX, Wang LJ (2016a) 5-Aminolevulinic acid thins pear fruits by inhibiting pollen tube growth via Ca2+-ATPase-mediated Ca2+ efflux. Front Plant Sci 7:121PubMedPubMedCentralGoogle Scholar
  4. An YY, Liu LB, Chen LH, Wang LJ (2016b) ALA inhibits ABA-induced stomatal closure via reducing H2O2 and Ca2+ levels in guard cells. Front Plant Sci 7:482PubMedPubMedCentralGoogle Scholar
  5. Apitz J, Nishimura K, Schmied J, Wolf A, Hedtke B, van Wijk KJ, Grimm B (2016) Posttranslational control of ALA synthesis includes GluTR degradation by Clp protease and stabilization by GluTR-binding protein. Plant Physiol 170(4):2040–2051CrossRefGoogle Scholar
  6. Balestrasse KB, Tomaro ML, Batlle A, Noriega GO (2010) The role of 5-aminolevulinic acid in the response to cold stress in soybean plants. Phytochemistry 71:2038–2045CrossRefGoogle Scholar
  7. Barrero-Gil J, Huertas R, Rambla JL, Granell A, Salinas J (2016) Tomato plants increase their tolerance to low temperature in a chilling acclimation process entailing comprehensive transcriptional and metabolic adjustments. Plant Cell Environ 39(10):2303–2318CrossRefGoogle Scholar
  8. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257CrossRefGoogle Scholar
  9. Cheng F, Lu JY, Gao M, Shi K, Kong QS, Huang Y, Bie ZL (2016) Redox signaling and CBF-responsive pathway are involved in salicylic acid-improved photosynthesis and growth under chilling stress in watermelon. Front Plant Sci 7:01519Google Scholar
  10. Czarnecki O, Hedtke B, Melzer M, Rothbart M, Richter A, Schroter Y, Pfannschmidt T, Grimm B (2011) An arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell 23:4476–4491CrossRefGoogle Scholar
  11. Dietz KJ, Mittler R, Noctor G (2016) Recent progress in understanding the role of reactive oxygen species in plant cell signaling. Plant Physiol 171:1535–1539CrossRefGoogle Scholar
  12. Dutilleul C, Garmier M, Noctor G, Mathieu C, Chétrit P, Foyer CH, Paepe Rd (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell 15:1212–1226CrossRefGoogle Scholar
  13. Elstner EF, Heupel A (1976) Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Anal Biochem 70:616–620CrossRefGoogle Scholar
  14. Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefGoogle Scholar
  15. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930CrossRefGoogle Scholar
  16. Guo XT, Li YS, Yu XC (2012) Promotive effects of 5-aminolevulinic acid on photosynthesis and chlorophyll fluorescence of tomato seedlings under suboptimal low temperature and suboptimal photon flux density stress. Hortic Sci 39(2):97–99Google Scholar
  17. Guy CL (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Annu Rev Plant Physiol Plant Mol Biol 41:187–223CrossRefGoogle Scholar
  18. Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611CrossRefGoogle Scholar
  19. Hodgins RR, Öquist G (1989) Porphyrin metabolism in chill-stressed seedlings of Scots pine (Pinus sylvestris). Physiol Plant 77:620–624CrossRefGoogle Scholar
  20. Hotta Y, Tanaka T, Takaoka H, Takeuchi Y, Konnai M (1997) New physiological effects of 5-aminolevulinic acid in plants: the increase of photosynthesis, chlorophyll content, and plant growth. Biosci Biotechnol Biochem 61:2025–2028CrossRefGoogle Scholar
  21. Knight MR, Knight H (2012) Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol 195:737–751CrossRefGoogle Scholar
  22. Korkmaz A, Korkmaz Y, Demirkıran AR (2010) Enhancing chilling stress tolerance of pepper seedlings by exogenous application of 5-aminolevulinic acid. Environ Exp Bot 67:495–501CrossRefGoogle Scholar
  23. Li D, Zhang J, Sun W, Li Q, Dai A, Bai J (2011) 5-Aminolevulinic acid pretreatment mitigates drought stress of cucumber leaves through altering antioxidant enzyme activity. Sci Hortic 130:820–828CrossRefGoogle Scholar
  24. Li QY, Lei S, Du KB, Li LZ, Pang XF, Wang ZC, Wei M, Fu S, Hu LM, Xu L (2016) RNA-seq based transcriptomic analysis uncovers α-linolenic acid and jasmonic acid biosynthesis pathways respond to cold acclimation in Camellia japonica. Sci Rep 6:36463CrossRefGoogle Scholar
  25. Li H, Chang JJ, Zheng JX, Dong YC, Liu Q, Yang XZ, Wei CH, Zhang Y, Ma JX, Zhang X (2017) Local melatonin application induces cold tolerance in distant organs of Citrullus lanatus L. via long distance transport. Sci Rep 7:40858CrossRefGoogle Scholar
  26. Liu D, Kong DD, Fu XK, Ali B, Xu L, Zhou WJ (2016) Influence of exogenous 5-aminolevulinic acid on chlorophyll synthesis and related gene expression in oilseed rape de-etiolated cotyledons under water-deficit stress. Photosynthetica 54:468–474CrossRefGoogle Scholar
  27. Liu T, Hu XH, Zhang J, Zhang JH, Du QJ, Li JM (2018a) H2O2 mediates ALA-induced glutathione and ascorbate accumulation in the perception and resistance to oxidative stress in Solanum lycopersicum at low temperatures. BMC Plant Biol 18:34CrossRefGoogle Scholar
  28. Liu T, Xu JJ, Li JM, Hu XH (2018b) NO is involved in JA- and H2O2-mediated ALA-induced oxidative stress tolerance at low temperatures in tomato. Environ Exp Bot. CrossRefGoogle Scholar
  29. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410CrossRefGoogle Scholar
  30. Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337CrossRefGoogle Scholar
  31. Naeem MS, Jin ZL, Wan GL, Liu D, Liu HB, Yoneyama K, Zhou WJ (2010) 5-Aminolevulinic acid improves photosynthetic gas exchange capacity and ion uptake under salinity stress in oilseed rape (Brassica napus L.). Plant Soil 332:405–415CrossRefGoogle Scholar
  32. Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Exogenous spermidine alleviates low temperature injury in mung bean (Vigna radiata L.) seedlings by modulating ascorbate–glutathione and glyoxalase pathway. Int J Mol Sci 16(12):30117–30132CrossRefGoogle Scholar
  33. Noctor G, Mhamdi A, Foyer CH (2016) Oxidative stress and antioxidative systems: recipes for successful data collection and interpretation. Plant Cell Environ 39:1140–1160CrossRefGoogle Scholar
  34. op den Camp RGL, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Gobel C, Feussner I, Nater M, Apel K (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15:2320–2332CrossRefGoogle Scholar
  35. Qu T, Liu RF, Wang W, An L, Chen T, Liu GX, Zhao ZG (2011) Brassinosteroids regulate pectin methylesterase activity and AtPME41 expression in Arabidopsis under chilling stress. Cryobiology 63(2):111–117CrossRefGoogle Scholar
  36. Richter AS, Grimm B (2013) Thiol-based redox control of enzymes involved in the tetrapyrrole biosynthesis pathway in plants. Front Plant Sci 4:371CrossRefGoogle Scholar
  37. Strain HH, Svec WA (1966) Extraction, separation, estimation and isolation of the chlorophylls. In: Vernon LP, Seeley GR (eds) The chlorophylls. Academic Press, New York, pp 21–66CrossRefGoogle Scholar
  38. Sun YP, Zhang ZP, Wang LJ (2009) Promotion of 5-aminolevulinic acid treatment on leaf photosynthesis is related with increase of antioxidant enzyme activity in watermelon seedlings grown under shade condition. Photosynthetica 47:347–354CrossRefGoogle Scholar
  39. Tanaka A, Tanaka R (2006) Chlorophyll metabolism. Curr Opin Plant Boil 9(3):248–255CrossRefGoogle Scholar
  40. Tewari AK, Tripathy BC (1998) Temperature-stress-induced impairment of chlorophyll biosynthetic reactions in cucumber and wheat. Plant Physiol 117:851–858CrossRefGoogle Scholar
  41. von Wettstein D, Gough S, Kananagara CG (1995) Chlorophyll biosynthesis. Plant Cell 7:1039–1105CrossRefGoogle Scholar
  42. Wang P, Grimm B (2015) Organization of chlorophyll biosynthesis and insertion of chlorophyll into the chlorophyll-binding proteins in chloroplasts. Photosynth Res 126(2–3):189–202CrossRefGoogle Scholar
  43. Wang LJ, Jiang WB, Huang BJ (2004) Promotion of 5-aminolevulinic acid on photosynthesis of melon (Cucumis melo) seedlings under low light and chilling stress conditions. Physiol Plant 121:258–264CrossRefGoogle Scholar
  44. Wang LJ, Jiang WB, Liu H, Liu WQ, Kang L, Hou XL (2005) Promotion by 5-aminolevulinic acid of germination of pakchoi (Brassica campestris ssp. chinensis var. communis Tsen et Lee) seeds under salt stress. J Integr Plant Biol 47:1084–1091CrossRefGoogle Scholar
  45. Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Montagu MV, Inzé D, Camp WV (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J 16(16):4806–4816CrossRefGoogle Scholar
  46. Willems P, Mhamdi A, Stael S, Storme V, Kerchev P, Noctor G, Gevaert K, Van Breusegem F (2016) The ROS wheel: refining ROS transcriptional footprints. Plant Physiol 171:1720–1733CrossRefGoogle Scholar
  47. Yang ZM, Chang ZL, Sun LH, Yu JJ, Huang BR (2014) Physiological and metabolic effects of 5-aminolevulinic acid for mitigating salinity stress in creeping bentgrass. PLoS One 9:e116283CrossRefGoogle Scholar
  48. Zhou WJ, Leul M (1998) Uniconazole-induced alleviation of freezing injury in relation to changes in hormonal balance, enzyme activities and lipid peroxidation in winter rape. Plant Growth Regul 26:41–47CrossRefGoogle Scholar
  49. Zhou Y, Zeng LT, Fu XM, Mei X, Cheng SH, Liao YY, Deng RF, Xu X, Jiang YM, Duan XW, Baldermann S, Yang ZY (2016) The sphingolipid biosynthetic enzyme Sphingolipid delta8 desaturase is important for chilling resistance of tomato. Sci Rep 6:38742CrossRefGoogle Scholar

Copyright information

© Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2018

Authors and Affiliations

  1. 1.College of HorticultureNorthwest A&F UniversityYanglingChina
  2. 2.Key Laboratory of Protected Horticultural Engineering in NorthwestMinistry of AgricultureYanglingChina

Personalised recommendations